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Limnetica, 29 (2): x-xx (2011)Limnetica, 33 (1): 73-88 (2014). DOI: 10.23818/limn.33.07c© Asociación Ibérica de Limnología, Madrid. Spain. ISSN: 0213-8409

Influence of the abiotic characteristics of sediments on the

macrobenthic community structure of the Minho estuary saltmarsh

(Portugal)

Thais C. Picanço1, C. Marisa R. Almeida1, Carlos Antunes1, 2, 3 and Pedro A. Reis 1, ∗

1 CIIMAR/CIMAR-Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Ruados Bragas, 289, 4050-123 Porto, Portugal.2 Aquamuseu do Rio Minho-Parque do Castelinho, 4920-290 Vila Nova de Cerveira, Portugal.3 Escola Superior Gallaecia-Largo das Oliveiras, 4920 Vila Nova de Cerveira, Portugal.

∗ Corresponding author: [email protected]

Received: 23/10/2013 Accepted: 05/02/2014

ABSTRACT

Influence of abiotic characteristics of sediments on the macrobenthic community structure of Minho estuary saltmarsh

(Portugal)

This work studied the spatial and seasonal variations of the macrobenthic community structure of the Minho estuary saltmarsh,which involved examining the relationships between the macrobenthic community and the abiotic characteristics of thesurrounding sediments: texture, organic matter content and metal (Cd, Cr, Cu, Fe, Ni, Pb and Zn) concentrations. These abioticcharacteristics showed significant ( p < 0.05) spatial and seasonal variations that demonstrated the complex sedimentarydynamics of this saltmarsh. The macrobenthic community structure consisted of 37 taxa belonging to 5 phyla: Annelida (10taxa), Mollusca (4 taxa), Arthropoda (21 taxa), Chordata (1 taxon) and Sipuncula (1 taxon). The mean annual abundancewas 1530 ind/m2, and the most abundant species were Cyathura carinata, Scolelepis squamata and Hediste diversicolor. Themacrobenthic community showed no standard spatial distribution throughout the saltmarsh, and species abundances showedhigh seasonal variations that were directly dependent on the natural environmental conditions of each season. Although theMinho estuary saltmarsh showed evidence of anthropogenic contamination by metals, the macrobenthic community was notsignificantly influenced by their presence, and the main structuring factor was the texture of the sediments.

Key words: Macrobenthic community, metal, saltmarsh, Minho river.

RESUMEN

Influencia de las características abióticas del sedimento en la estructura de la comunidad macrobentónica del estuario del

Río Minho (Portugal)

Este trabajo ha estudiado las variaciones espaciales y estacionales de la estructura de la comunidad macrobentónica del

estuario del río Miño, incluyendo el estudio de las relaciones entre la comunidad macrobentónica y las características

abióticas de los sedimentos: textura, contenido de materia orgánica y concentraciones de metales (Cd, Cr, Cu, Fe, Ni, Pb y Zn).

Estas características abióticas han mostrado variaciones espaciales y estacionales significativas (p < 0.05), demostrando

las complejas dinámicas sedimentarias de este estuario. La estructura de la comunidad macrobentónica fue constituida por

treinta y siete taxa de cinco phyla: Annelida (diez taxa), Mollusca (cuatro taxa), Arthropoda (veintiuna taxa), Chordata (un

taxon) y Sipuncula (un taxon). La media de la abundancia anual fue de 1530 ind/m2 y las especies más abundantes fueron

Cyathura carinata, Scolelepis squamata y Hediste diversicolor. La comunidad macrobentónica no mostró una distribución

espacial estándar a lo largo del estuario y sus abundancias mostraron elevadas variaciones estacionales directamente

dependientes de las condiciones ambientales de cada estación. A pesar de que el estuario del Miño mostró evidencias de

contaminación de metales de origen antropogénico, la comunidad macrobentónica no se vio significativamente afectada y el

mayor factor estructural fue la textura de los sedimentos.

Palabras clave: Comunidad macrobentónica, metales, estuario, río Miño.

15293 Limnetica 33(1), pàgina 73, 15/05/2014

74 Picanço et al.

INTRODUCTION

The study of macrobenthic community structuresand their dynamics has been an ecological prior-ity, as benthic faunal activities affect and regulatethe physicochemical and biological processes ofestuarine systems (Day et al., 1989). The mac-robenthic community structure is also consideredto be a useful instrument in the elaboration ofecological quality studies and environmental di-agnostics, as it can reflect with high precision theprevious environmental conditions of the ecosys-tem (Warwick, 1986; Lana, 1994). This useful-ness can be related to the presence of macroben-thic species near the bottom of ecosystems or insediments, as well as their low mobility (Canfieldet al., 1994; Weisberg et al., 1997; Clarke & Gor-ley, 2001). The characterization of macrobenthiccommunity structures should include the study ofspecies abundances, diversity and evenness in-dices (Farinha & Trindade, 1994; Alves, 1996and 2000; Gamboa, 1999; Mucha et al., 2003).Then, multivariate analyses can indicate the spa-tial and seasonal variations of the communityand the influence of sediment abiotic character-istics (e.g., texture, organic contents and pollu-tants such as metals) in its distribution throughoutthe ecosystem during different seasons (Farinha &Trindade, 1994; Alves, 1996 and 2000; Gamboa,1999; Mucha et al., 2003; Reis et al., 2009).

Estuarine saltmarsh areas are excellent nurs-ery and protection regions, but they can alsoaccumulate high contaminant concentrations intheir sediments and plants (Teal, 1986; Vale et

al., 1990; Reis et al., 2009). Consequently, es-tuarine community structures can be influencedby geological and anthropogenic gradients ofcontamination, particularly of metals (Pearson& Rosenberg, 1978; Rakocinski et al., 1997).However, the geological contribution of met-als complicates the identification of potentialsources of contamination and makes the inter-pretation of their disturbing effects significantlymore difficult (Weisberg et al., 1997; Gaston& Nasci, 1998; Mucha et al., 2003; Reis et al.,2009). Furthermore, the challenge of detectinganthropogenic impacts in naturally stressedsystems such as estuaries and saltmarshes using

biological assessment methods and indices isconsidered as a Quality Paradox (Dauvin, 2007;Elliott & Quintino, 2007).

The international section of the Minho River(including its saltmarsh area) was classified asa Natura 2000 location. The saltmarsh area isparticularly important to avifauna, about whichsome scientific knowledge is available (Far-inha & Trindade, 1994; Alves, 1996 and 2000;Gamboa, 1999). However, the composition anddistribution of the subtidal macrozoobenthiccommunity present in the saltmarsh area ofthe Minho Estuary remain unknown. Previouswork has shown the importance of sediments insaltmarsh areas as sinks for contaminants such asheavy metals, and coupled with the potential ofthe macrozoobenthic community to transfer thispollution to higher trophic levels, the conditionssuggest that a biogeochemical study approach isappropriate (Reis et al., 2009 and Mil-Homenset al., 2013a, b). Such biogeochemical studiesare very scarce in Portuguese estuaries, and nonehave been reported in the particular case of thesingle saltmarsh existing in the Minho estuary.

Thus, the major aims of this work wereto study the Minho estuary saltmarsh over aone-year period, determining the patterns of themacrozoobenthic community composition inrelation to (i) the influence of the abiotic charac-teristics of sediments (texture, organic contentsand metal concentrations) and (ii) species abun-dance, biomass and diversity. These data may beused to evaluate the importance of this particulararea of the estuary for conservation purposes.

MATERIALS AND METHODS

Study Area

The Minho estuary is located in the northwest(NW) region of Portugal and includes a varietyof habitats with great environmental value, suchas its saltmarsh areas (at the junction of the riversMinho and Coura, near Caminha village) (Far-inha & Trindade, 1994; Alves, 1996 and 2000;Gamboa, 1999). Indeed, the Minho estuary salt-marsh was considered as a metal pristine area by


Changes on the macrobiotic community structure of the Minho estuary saltmarsh 75

Reis et al. (2009), although the increase of localindustrial and tourism (fishing and cruising) ac-tivities has introduced anthropogenic sources ofmetals into this ecosystem. The river Minho is300 km long, and the 70 km furthest downstreamare considered to be a natural boundary betweenPortugal and Spain; the area is usually referred toas the international section (Sousa et al., 2008).The river flows westward from the north of Spain(Cantabrian Mountains) and discharges into theAtlantic Ocean with an average annual flow rateof 300 m3/s (Sousa et al., 2013). The total areaof the Minho watershed is approx. 17100 km2,but only 23 km2 are estuarine area (Sousa et al.,2008). The Minho estuary is part of a Natura2000 site, which includes the entire internationalsection of the river (Sousa et al., 2008). Addi-tionally, the Coura River extends over 10 km in

length and reaches the Minho estuary saltmarsh2 km before the estuary mouth, with an annualaverage flow rate of 10 m3/s (Sousa et al., 2013).We selected 10 sampling sites according to thesalinity gradient during high tide and their spatiallocations (interior and exterior area) in the salt-marsh (Fig. 1), from which sediments were col-lected for assessing the macrobenthic communitystructures (abundances, diversity and evenness).The mean distances between the sampling siteswere 800 m along the river Coura (sites 1-4) and230 m in the interior areas (sites 5-10), coveringa total saltmarsh area of 1.04 km2. Samples werealso collected at these sites to assess the abioticcharacteristics of their waters (near bottom: tem-perature, dissolved oxygen and salinity) and sed-iments (texture, organic contents and metal con-centrations).

Figure 1. Locations of the 10 sampling sites in the Minho estuary saltmarsh (Portugal), near Caminha village (adapted from Reis et

al., 2009). Localización de los diez puntos de muestreo en el estuario del río Miño (Portugal), cerca de la villa de Camiña (adaptado

de Reis et al., 2009).


76 Picanço et al.

Reagents and materials

The reagents and materials used in this studyhave been previously described by Reis et al.

(2009): (i) the concentrated nitric acid (Fluka,pro analysis, without further purification) and theremaining reagents were of pro analysis level;(ii) ultrapure water (Milli-Q level, Millipore Sys-tems) was used to prepare all solutions; (iii) Stan-dard Reference Material certified for “Inorgan-ics in Marine Sediment” (SRM 2702, NIST) wasused to verify the suitability of the digestion pro-cedure and of the optimized analytical methodfor the metal analyses in the sediments; and (iv)the material used in the sampling collections andtreatments had been previously decontaminatedin a 20 % (v/v) nitric acid solution.

Sampling strategy and analytical methods

Independent sediment replicates (n = 4) werecollected using a Van Veen grab (area of 500 cm2

and a maximum capacity of 5000 cm3) at eachsite in September 2005 (summer), December2005 (autumn) and March 2006 (winter) forabiotic and biotic characterization.

The analytical methods used to study the abioticcharacteristics (texture, organic matter contentsand metal concentrations) of the sediments havebeen previously described by Reis et al (2009).For texture characterization, the sediment sampleswere dried in an oven at 60 ◦C for 48 hours,and dimensional analyses were conducted using aRo-Tap sieves system. The weight of each class(gravel: > 2 mm; very coarse sand: 1-2 mm; coarsesand: 0.500-1 mm; medium sand: 0.250-0.500 mm;fine sand: 0.125-0.250 mm; very fine sand:< 0.125 mm; and clay and silts: < 0.063 mm)was expressed as a percentage (%) of totalweight. The organic matter content was deter-mined after combustion of the sediment samplesin a furnace at 550 ◦C for 24 hours, and the valueswere expressed as percentages (%) relative tothe initial sample weight. The metal (Cd, Cr, Cu,Fe, Ni, Pb and Zn) analyses have been describedby Reis et al. (2009): digestion in Teflon vessels(model 4782, Parr) in a microwave system(model 440, Panasonic). The metal concentra-

tions were determined by Atomic AbsorptionSpectrometry (SpectrAA 220 FS, Varian), cou-pled with a deuterium lamp as a backgroundcorrector, using flame atomization (Marck 7, Var-ian) and electrothermal atomization (GTA 110,Varian), depending on the metal concentrationsin the samples (Reis et al., 2009). An adequateapproach to study the potential anthropogeniccontamination of sediments by metals is thenormalization of these elements using a refer-ence element not associated with contamination,such as Al, Li or Fe (Schiff & Weisberg, 1999;Mucha et al., 2003; Reis et al., 2009). The studyof Reis et al. (2009) used Fe as a conservativeindicator for the following reasons: (i) Fe is thefourth-most-abundant metal on earth (with amean concentration in superficial terrestrial sed-iments of 3.5 %); (ii) normally, anthropogenicsources of Fe are scarce compared with naturalFe concentrations; and (iii) the ratios betweenother metals and Fe are nearly constant in ter-restrial sediments (Velinsky et al., 1994). Reiset al. (2009) showed that some interior areas ofthis saltmarsh had evidence of anthropogeniccontamination by metals (Cr, Cu, Ni and Pb).

For biotic characterization, the sediment sam-ples were fixed with a buffered seawater-formalinsolution (10 %, v/v) and sieved through a 1 mmmesh for the separation of macrobenthic organisms.Then, the samples were preserved in an ethanolsolution (70 %, v/v) with Rose Bengal (as stain-ing agent), and the organisms were counted andidentified to the lowest possible taxon, normallythe species level (Gaston & Nasci, 1998).

Data analyses

Individual species abundance and biomass wereexpressed per square metre. Measures includedabundance, biomass, number of species (S),Shannon-Wiener diversity index (H′) and Pie-lou’s evenness (J′) index. Principal ComponentAnalysis (PCA) was used to detect habitat differ-ences based on the abiotic data and to establishcorrelations between biological parameters andabiotic characteristics; the indices of abiotic andbiotic similarity were compared using BIO-ENV(using the Spearman coefficient) (Clarke & War-



wick, 1994). For statistical analyses of the bioticvalues, cluster multivariable analyses allowed forthe study of the spatial and seasonal variations ofspecies distributions (using SPSS software). Forthe statistical analyses of the abiotic values (or-

ganic matter contents and metal concentrationsin the sediments), the following sequence ofsteps was conducted: (i) the normality of the datawas checked by the Shapiro-Wilk test, consider-ing one level of significance ( p < 0.05), using

Table 1. The physicochemical parameters of the waters, as well as the texture and organic matter contents of the sediments, ofthe Minho estuary saltmarsh obtained for the three sampling dates. Temperature (T, ◦C), dissolved oxygen (DO, mg·L–1), salinity(S, psu), gravel (G, %), vary coarse sand (VCS, %), coarse sand (CS, %), medium sand (MS, %), fine sand (FS, %), very fine sand(VFS, %), silt + clay (S+C, %) and organic matter (OM, %). Parámetros físico-químicos del agua, materia orgánica y textura de

los sedimentos en el estuario del río Miño, obtenidos a lo largo de los tres muestreos. Temperatura (T, ◦C), oxígeno disuelto (DO,

mg·L–1), salinidad (S, psu), grava (G, %), arena muy gruesa (VCS, %), arena gruesa (CS, %), arena media (MS, %), arena fina (FS,%), arena muy fina (VFS, %), limo + arcilla (S+C, %) y materia orgánica (OM, %).

Summer

Sampling Site 1 2 3 4 5 6 7 8 9 10

T 14.2 16.0 19.2 14.3 14.9 15.4 15.9 17.2 15.7 17.6DO 9.0 10.0 9.5 8.3 8.2 8.4 8.0 8.2 8.2 7.5S 34.4 29.4 16.9 33.5 33.4 32.0 31.0 29.0 31.0 24.7

G 2.4 38.6 60.9 21.9 4.1 51.9 8.7 4.1 0.1 5.0VCS 7.8 35.5 22.2 29.4 9.9 16.7 10.3 8.2 0.5 8.0CS 34.4 20.7 13.7 23.9 24.3 15.9 27.1 26.3 9.7 8.5MS 20.6 4.1 2.5 21.5 19.6 12.9 39.7 35.8 27.1 29.9FS 19.3 0.7 0.4 2.2 11.5 0.9 6.3 13.9 23.6 10.3

VFS 13.6 0.2 0.1 0.6 15.5 0.2 4.2 5.2 18.3 1.5S + C 2.0 0.2 0.2 0.5 15.1 1.3 3.6 6.5 20.6 36.9

OM 3.0 1.2 1.2 1.2 10.0 4.4 2.1 4.0 8.0 2.8

Autumn

T 13.4 9.9 10.7 12.1 9.0 8.7 13.0 11.6 9.1 8.7DO 7.0 11.0 9.9 11.1 10.8 9.8 9.5 7.0 7.6 7.4S 33.5 0.5 0.0 26.0 5.0 7.5 31.8 25.0 4.4 1.9

G 8.1 77.0 3.6 38.7 11.6 5.9 16.6 4.6 0.8 0.9VCS 24.9 9.0 11.8 25.0 14.0 15.0 26.0 15.4 1.0 4.5CS 49.3 3.0 60.6 16.6 20.4 25.2 25.8 18.8 3.0 20.2MS 10.5 0.0 19.9 10.5 36.2 30.9 18.2 23.0 8.8 44.0FS 4.1 1.0 2.7 4.2 10.7 12.8 7.9 17.8 35.2 18.5

VFS 2.3 5.0 1.0 2.2 3.5 6.2 3.8 7.5 35.0 6.8S + C 0.8 5.0 0.4 2.8 3.7 4.1 1.6 13.0 16.2 4.9

OM 1.7 1.4 1.3 2.7 3.3 6.9 1.9 5.2 11.2 8.2

Winter

T 13.2 12.3 12.0 11.7 12.8 12.9 13.1 12.5 11.7 12.4DO 9.1 10.8 10.8 11.0 10.9 11.0 9.0 9.6 11.5 11.1S 32.8 0.1 0.0 3.6 0.3 0.8 32.6 25.0 1.1 0.6

G 70.3 81.8 9.9 38.3 1.6 9.7 15.1 7.0 0.2 4.9VCS 15.6 9.8 46.4 33.6 4.6 7.9 21.0 10.7 1.5 6.2CS 10.8 6.0 39.4 18.1 7.9 17.7 22.3 21.8 19.6 10.7MS 1.9 1.3 3.8 8.1 15.5 23.6 19.8 38.3 44.8 49.8FS 0.5 0.4 0.2 1.3 22.9 16.9 15.5 12.4 16.9 20.0

VFS 0.5 0.3 0.2 0.3 29.6 13.0 4.6 4.7 9.4 4.8S + C 0.4 0.4 0.2 0.3 18.0 11.3 1.6 5.1 7.5 3.6

OM 1.3 1.5 1.1 1.2 11.3 11.0 1.5 3.8 5.1 2.2


78 Picanço et al.

SPSS software; (ii) because some values failedthe normality tests, all data were logarithmically(base 10) transformed to reduce deviations fromthe normal distribution; (iii) the homogeneityof variances was checked by the Cochran test,considering one level of significance ( p < 0.05),using WinGMAv 5 software (EICC, Universityof Sydney); (iv) two-way analyses of variance(ANOVA) were used to identify significant spa-tial and seasonal differences ( p < 0.05) usingWinGMAv 5 software (EICC, University of Syd-ney); and (v) unplanned comparisons (post hoctests) were conducted to establish groups ofsampling sites and seasons which differed signi-ficantly ( p < 0.05) using the Student-Newman-Keuls (SNK) test for ANOVAs from WinGMAv5 software (EICC, University of Sydney).

RESULTS AND DISCUSSION

Environmental analyses

Physicochemical parameters of waters and the

texture and organic matter contents of sediments

The physicochemical parameters of the waterswere directly influenced by the typical character-istics of each season and tide period: (i) highertemperatures and salinities during summer andat sampling sites more exposed to marine intru-sion during high tide and (ii) lower temperaturesand salinities during winter and at sites more ex-posed to fresh waters from the Coura River (Ta-ble 1). The dissolved oxygen concentrations werealways higher than 7.0 mg·L−1 for the three sam-pling dates, which indicated optimum concentra-tions (DO ≥ 6.0 mg·L−1 at 15 ◦C) and well-mixedbody waters (Reis et al., 2009). A number ofsampling sites (i.e., sites 2-6 during winter) hadsaturated dissolved oxygen concentrations (DO ≥10.0 mg·L−1 at 15 ◦C), suggesting excellent eco-logical qualities (Reis et al., 2009).

The textures of the sediments were constantacross the saltmarsh during all seasons (except atsite 7):

(i) gravel (> 2 mm) and very coarse sand (1-2mm) fractions dominated at sites 1, 2, 3 and4 (Coura River mainstream);

(ii) very fine sand (<0.125 mm) and clay andsilts (< 0.063 mm) fractions dominated atsite 5 (interior saltmarsh);

(iii) fine sand fraction (0.125-0.250 mm) domi-nated at sites 6, 8, 9 and 10 (medium salt-marsh);

(iv) site 7 (interior saltmarsh) showed high sea-sonal variation, with the very fine sand, clayand silt fractions dominant during summerand the gravel and coarse sand fractionsdominant during the autumn and winter.This result may be due to the higher riversflows during autumn and winter, whichcould transport the finer sediments fromthis site to adjacent protected areas (sites5-6 and 8-10).

These sediment textures were similar to thoseof other European estuaries: coarser sediments inthe river areas (mainly in the Coura River: lo-cations 1-4) and finer sediments in the protectedinterior areas (Diez, 1980; Mora, 1980; Asensio& Gómez, 1984). Normally, these interior areas(locations 5-10) can retain finer sediments andhave higher floral biomasses, which contribute tothe formation of natural barriers that slow downwater flows and accumulate high concentrationsof metals (Diez, 1980; Mora, 1980; Asensio &Gómez, 1984).

The saltmarsh areas with the finer sedimentscorresponded to the areas with the highest or-ganic matter contents (Table 1). Normally, theseareas also have a higher ability to retain contam-inants in chemical forms that are more availableto organisms, such as metals (Chapman & Wang,2001). As expected, organic matter contents werehighest in the sediments of site 5, lowest at sites1-4 and intermediate at sites 6 and 8-10 duringall seasons. Only the sediments of site 7 suffereda high reduction of organic matter contents fromsummer to autumn and winter, which coincidedwith the change of texture.

Heavy metal concentrations in sediments

The metal (Cd, Cr, Cu, Fe, Ni, Pb and Zn) con-centrations in the sediments of the Minho estu-ary saltmarsh showed significant spatial and sea-



sonal variations (Fig. 2 and Table 2). Detailedmeasurements of metal concentrations obtainedin September 2005 (summer) can be found inReis et al. (2009).

The limits of detection were calculated ac-cording to the APHA recommendations (Sedi-ments (mg·kg−1, dry wt): Cd: 0.0041; Cr: 5.0; Cu:0.046; Fe (%): 0.25; Mn: 4.1; Pb: 0.099 and Zn:9.1) (APHA, 1998; Reis et al., 2009). The anal-yses of the SRM 2702 showed acceptable meanrecoveries for all of the metals: Cd (117.6 %), Cr(75.4 %), Cu (89.3 %), Fe (83.1 %), Pb (94.2 %)and Zn (92.5 %), except for Ni (70.5 %). Al-though the digestion procedure did not allow forthe complete dissolution of the sediment sam-

ples, digestion with only concentrated nitric acidis indicative of metal levels that are more envi-ronmentally bioavailable and have higher ecotox-icological potential (EPA, 1994).

The ANOVAs of the metal concentrations re-sulted in three significantly ( p < 0.05) differentclusters of sampling sites: (i) Group A with highmetal concentrations, which included sites 5, 7and 9; Group B with intermediate metal concen-trations, which included sites 1, 6, 8 and 10; andGroup C with low metal concentrations, whichincluded sites 2, 3 and 4 (Fig. 2). These spatialdistributions were directly influenced by the nat-ural characteristics of the sediments of each sam-pling site at each season, as the sites with higher

Table 2. Two-way analyses of variance (ANOVAs) of metal (Cd, Cr, Cu, Fe, Ni, Pb and Zn) concentrations in the sediments ofMinho estuary saltmarsh obtained for the three sampling dates, which allowed for the identification of significant spatial and seasonaldifferences ( p < 0.05) using WinGMAv 5 software (EICC, University of Sydney). In each season, different letters shows significantspatial differences ( p < 0.05): increasing order of concentrations is A<B<C, etc. In each location, different numbers showssignificant temporal differences ( p < 0.05): increasing order of concentrations is 1< 2< 3, etc. Análisis de varianza de dos vías

(ANOVA) de las concentraciones de metales (Cd, Cr, Cu, Fe, Ni, Pb y Zn) de los sedimentos del estuario del río Miño, obtenidos a lo

largo de los tres muestreos realizados, el cual ha permitido identificar diferencias espaciales y estacionales significativas (p < 0.05):el orden de concentraciones crecientes es A<B<C, etc. En cada punto de muestreo, los diferentes números muestran diferencias

temporales significativas (p < 0.05): el orden de concentraciones crecientes es 1< 2< 3, etc.

ANOVAS of metal concentrations in sediments of Minho estuary saltmarsh

Metal Sampling Season 1 2 3 4 5 6 7 8 9 10

Cd

Summer D,E,2 A,1 B,1 B,C,2 F,1 E,1 F,2 D,E,2 F,2 C,D,1Autumn B,2 B,3 B,1 B,2 D,1 C,1 A,1 B,1 E,3 B,C,1Winter A,B,1 A,B,2 B,1 A,1 D,1 C,1 B,1 C,1,2 C,D,1 C,1

Cr

Summer A,B,1 A,B,1 A,1 A,1 D,1 B,C,1 D,3 D,3 C,D,1 B,1Autumn A,B,1 A,B,1 A,1 A,B,1 C,1 A,B,1 A,B,1 A,B,1 C,1 B,C,1Winter B,2 B,2 A,1 A,1 D,2 C,2 C,2 B,C,2 B,C,1 B,C,2

Cu

Summer B,2 B,1 B,1 A,1 D,1 C,1 D,2 C,1 D,2 B,1Autumn A,1 D,2 B,C,D,1 A,B,C,2 E,1 D,1 A,B,1 C,D,1 F,3 D,2Winter B,C,D,2 B,C,1 B,1 A,1 F,2 C,D,E,1 D,1 E,1 E,1 D,E,2

Pb

Summer A,1 A,1 A,1 A,1 D,1 B,2 C,2 B,2 C,2 B,2Autumn A,1 A,1,2 A,3 B,2 D,1 C,2 A,1 A,1 E,3 A,1Winter D,2 B,C,D,2 B,C,D,2 A,B,1 E,2 A,1 B,C,D,1 C,D,1,2 A,B,C,1 A,B,C,1

Ni

Summer B,2 A,1 A,1 A,2 E,1 D,1 F,3 D,1 E,2 B,C,1Autumn A,1 A,B,1 A,1 A,B,2 D,1 C,D,1 B,1 C,D,1 E,2 D,2Winter B,2 B,2 A,1 A,1 E,2 C,D,1 C,2 C,D,1 D,1 C,D,2

Zn

Summer A,B,C,1 A,B,C,1 A,B,1 A,1 E,1 C,D,1 D,E,2 C,D,1 E,2 B,1Autumn A,1 A,B,1 A,B,1 A,1 C,D,1 A,B,1 A,B,1 A,B,1 D,2 B,C,2Winter B,1 B,1 B,1 A,1 C,1 B,1 B,1 B,1 B,1 B,1

Fe

Summer A,B,1,2 B,C,1 A,1 A,1 E,1 D,1 E,2 B,C,D,1 F,2 C,D,1Autumn A,1 B,1 B,2 A,1 D,1 B,C,1 B,1 B,1 E,3 C,1Winter B,C,2 B,C,1 B,1 A,1 E,2 D,1 B,C,1 B,C,1 E,1 C,1


80 Picanço et al.

metal concentrations had finer sediments andhigher organic matter contents. This observationwas corroborated by the seasonal variations ofmetal concentrations (Fig. 2 and Table 2: differ-ent numbers represent significant seasonal vari-ations in each location), which also coincidedwith the variations of texture and organic mattercontents between seasons. For example, the sedi-ments of site 7 showed a great reduction of metalconcentrations from summer to winter, which co-incided with the reduction of their very fine sand,clay and silt fractions and organic matter contents.

The geological characteristics of the sedi-ments complicate the distinction between naturaland anthropogenic sources of organic and in-organic contaminants. An adequate approachto distinguish organic from inorganic contami-nation and natural from anthropogenic sourcesis the normalization of vestigial metals using amacroelement such as Al, Li or Fe (Mucha et al.,2003; Reis et al., 2009). Reis et al. (2009) already

performed these normalizations in the sedimentsof the Minho estuary saltmarsh and revealed thatsites 5 and 7 (interior saltmarsh areas) showedevidence of anthropogenic contamination byCr, Cu, Ni and Pb during summer (minimumflows and metal dilution factors), but only site5 continued to show that contamination duringwinter (maximum flows and metal dilutionfactors). These results suggest that the metalconcentrations obtained in the sediments of theMinho estuary saltmarsh were not exclusivelyderived from natural sources, and these anthro-pogenic contributions might have also influencedthe macrobenthic community structure of thissaltmarsh. However, comparisons with othernational wetlands have shown that the sedimentsof Minho estuary saltmarsh have much lowermetal concentrations, being similar only to RiaFormosa (a summary table of metal concentrationsin the superficial sediments of different Portuguesewetlands can be found in Reis et al. (2009).

0

100

200

300

400

1 2 3 4 5 6 7 8 9 10

Co

nc

(µ

g/k

g)

Cd

0,0

10,0

20,0

30,0

40,0

1 2 3 4 5 6 7 8 9 10

Co

nc

(m

g/k

g)

Cr

0,0

10,0

20,0

30,0

40,0

1 2 3 4 5 6 7 8 9 10

Co

nc

(m

g/k

g)

Cu

0,0

1,5

3,0

4,5

6,0

1 2 3 4 5 6 7 8 9 10

Co

nc

(%

)

Sampling Site

Fe

Summer Autumn Winter

0,0

7,5

15,0

22,5

30,0

1 2 3 4 5 6 7 8 9 10

Co

nc

(m

g/k

g)

Ni

0,0

7,5

15,0

22,5

30,0

1 2 3 4 5 6 7 8 9 10

Co

nc

(m

g/k

g)

Pb

0,0

30,0

60,0

90,0

120,0

1 2 3 4 5 6 7 8 9 10

Co

nc

(m

g/k

g)

Sampling Site

Zn

Summer Autumn Winter

Figure 2. Metal concentrations (Cd, Cr, Cu, Fe, Ni, Pb and Zn) of the sediments collected from each sampling site during eachsampling trip. Concentración de metales (Cd, Cr, Cu, Fe, Ni, Pb y Zn) en los sedimentos recogidos en cada punto de muestreo,

durante cada muestreo.



Biological analyses

Macrozoobenthos Abundance, Diversity

and Evenness

In the Minho estuary saltmarsh, a total of 10

185 individuals were identified during the three

sampling dates, distributed across 5 phyla and

37 taxa: Annelida (10 taxa), Mollusca (4 taxa),

Arthropoda (21 taxa), Chordata (1 taxon) and Si-

puncula (1 taxon) (Appendix 1, available: www.

limnetica.net/internet).

The mean annual abundance (per area unit)

of the three sampling dates was 1530 ind/m2.

The highest total abundance (6330 ind/m2 of

nine different species) was observed at site 4

(Coura River mainstream) during summer (the

peak of the macrobenthic recruitment season,

with a total mean abundance of 1977.5 ind/m2).

Site 4 presented sediments dominated by gravel

and very coarse sand, low organic matter con-

tents and minimum metal concentrations, which

might represent an ideal uncontaminated area

to macrobenthos. The lowest total abundance

(95.0 ind/m2 of 3 different species) was obtained

at site 10 (intermediate saltmarsh) during win-

ter (severe hydrodynamic conditions, with a total

mean abundance of 744.0 ind/m2); this result can

be directly related to the typical life cycle of the

benthic species in the Minho estuary, which have

their optimum recruitment periods during sum-

mer (Sousa et al., 2008). The sediments of site

10 were dominated by the fine sand fraction and

had medium organic matter content, with no ev-

idence of anthropogenic contamination by met-

als. Indeed, two sampling sites (4 and 10) con-

sidered to be uncontaminated by metals showed

completely different total abundances. This result

suggested that macrobenthic community struc-

ture was more dependent on the texture and or-

ganic matter contents typical of each season than

on metal concentrations.

The species diversity of this saltmarsh showed

no consistent pattern among the different sam-

pling sites and seasons (Appendix 1, www.limne-

tica.net/internet and Table 3). However, the great-

est number of different species of macrobenthos

was observed in the Coura River mainstream

Table 3. Values of species number (S), Shannon-Wiener diversity index (log H′) and evenness index (J′) of the Minho estuarysaltmarsh obtained for the three sampling dates. Valores del número de especies (S), índice de diversidad de Shannon-Weaver (log H′)e índice de homogeneidad (J′) del estuario del río Miño a lo largo de los tres muestreos.

Number of Species (S)

Sampling Site 1 2 3 4 5 6 7 8 9 10

Summer 13 10 14 9 13 11 9 8 6 10

Autumn 10 13 17 11 11 7 9 8 6 5

Winter 13 14 14 8 9 6 7 11 6 3

Shannon-Weaver Diversity Index (log H′)

Sampling Site 1 2 3 4 5 6 7 8 9 10

Summer 1.40 1.50 1.71 1.61 1.37 1.27 1.50 1.71 1.01 1.51

Autumn 1.79 1.82 1.70 1.23 1.18 1.55 1.33 1.47 0.84 1.10

Winter 1.25 1.25 1.94 1.11 1.52 1.48 1.34 1.87 0.79 0.91

Evenness Index (J′)

Sampling Site 1 2 3 4 5 6 7 8 9 10

Summer 0.55 0.65 0.65 0.73 0.53 0.53 0.68 0.82 0.56 0.66

Autumn 0.78 0.71 0.60 0.51 0.49 0.79 0.61 0.71 0.47 0.69

Winter 0.49 0.47 0.74 0.53 0.69 0.83 0.69 0.78 0.44 0.83


http://www.limnetica.net/internet



82 Picanço et al.

(sites 1-3) during all seasons, particularly at site3, which had 17 different species during autumn.The remaining sites 5-10 showed only a fewdifferent species and had low Shannon-Wienerdiversity indices, especially site 10, which hadonly 3 different species during winter. Oncemore, this result suggested that the texture andorganic matter contents of the sediments werethe main structuring factors of this macrobenthiccommunity.

Although the species richness of the saltmarshcan be estimated by the number of species and

the Shannon-Wiener diversity indices, the rel-ative species abundance should be assessed byevenness indices (Table 3). These evenness in-dices (0 ≤ J′ ≤ 1) were at their maximum andminimum, respectively, in site 10 (J′ = 0.83) andsite 9 (J′ = 0.44) during winter. Higher values ofevenness indicate a more homogeneous commu-nity structure and less diversity. Thus, the higherevenness values of the interior saltmarsh areas(sites 6, 8 and 10) indicated that these areas wereless adapted to severe ecological changes. The re-maining sites (1-5 and 7) showed intermediate

Table 4. Cluster Multivariable Analysis: mean similarity between groups, total abundance and dominant species per faunal group.The group G1 was established without a mean similarity or species dominance. Numbers represent the sampling sites (1-10),and letters represent the sampling seasons (S-Summer; A-Autumn; W-Winter). BIO-ENV analysis of the abiotic factors (texture,organic matter contents and metal concentrations) of the sediments of the Minho estuary saltmarsh obtained for the three samplingdates. Análisis de agrupamiento multivariante: similaridad media entre grupos, abundancia total y especies dominantes por grupo

faunístico. El grupo G1 fue establecido en similitud media o especie dominante. Los números representan puntos de muestreo (1-10)

y las letras representan épocas de muestreo (S-verano; A-otoño; W-invierno). Análisis BIOENV de los factores abióticos (textura,

materia orgánica y concentraciones de metales) de los sedimentos del estuario del río Miño a lo largo de los tres muestreos.

Faunistic

Group

CLUSTER ANALYSIS

Site-Season Mean Similarity

(%)

Total Abundance

(%)

Species Dominance Contribution

(%)

Total Contribution

(%)

Group G1 10-W — 2.39 — — —

Group G2

2-S/A/W

34.47 41.29

Cyathura carinata 44.68

59.143-S/A/W4-A10-S

Corophium sp. 14.46

Group G3

5-S/A

36.78 31.32

Scolelepis squamata 32,37

63.696-S/A/W8-S/A/W

10-AAlkmaria romijni 31.32

Group G4

1-S/A/W

39.86 25.00

Hediste diversicolor 59.57

82.604-S/W5-W

7-S/A/W9-S/A/W

Scolelepis squamata 23.03

Number of

VariablesBIOENV ANALYSIS-BEST VARIABLES COMBINATION

1

0.311

Fine Sand(0.125-0.250 mm)

0.261

Organic Matter(MO)

0.249

Median Sand(0.250-0.500 mm)

2

0.350

Fine Sand + Coarse Sand(0.125-0.250/0.500-1 mm)

0.346

Fine Sand + Organic Matter(0.125-0.250 mm + MO)

0.331

Median Sand + Organic Matter(0.250-0.500 mm + MO)

3

0.382

Fine Sand + Coarse Sand +Organic Matter

(0.125-0.250/0.500-1 mm + MO)

0.379

Median Sand + Coarse Sand +Organic Matter

(0.250-1 mm + MO)

0.363

Fine Sand + Median Sand + Coarse Sand(0.125-1 mm)



evenness values during all seasons, which sug-gested that the macrobenthic community in theseareas could potentially adapt and survive moreeasily to new environmental conditions.

The mean abundance, diversity and evennessvalues found in the Minho estuary saltmarsh inthis study were much lower than those reportedby Sousa et al. (2008) along the Minho Rivermainstream gradient in 2006 (Abundance =3716 ind/m2; n = 28 different species; Shan-non-Wiener index (H′) = 1.36 and Pielou even-ness index (J′) = 0.41), which reinforces the ideathat macrobenthic community structure of thesesaltmarsh areas is being influenced by anthro-pogenic metal contamination. However, com-parisons with other European estuaries haveshown that the Minho estuary saltmarsh iscolonized by the typical marine macrobenthosspecies associated with sandy sediments with loworganic matter contents (Attrill et al., 1996; Run-dle et al., 1998; Bruyndoncx et al., 2002; Yse-baert et al., 2002, 2003 and Sousa et al., 2008;).Normally, these marine downstream areas havelow abundance and diversity values becausesandier ecosystems cannot sustain rich macroben-thic communities (Vasconcelos & Cerqueira, 2001;Sousa et al., 2008 and Costa-Dias et al., 2010).

Macrozoobenthos community composition

The cluster multivariable analyses constructedfour significantly different faunal groups (G1,G2, G3 and G4) in the saltmarsh (Table 4).

The group G1 (winter: site 10) was establishedwithout a mean similarity or species dominancevalue and represents 2.39 % of the total abun-dance of macrobenthic community. As expected,site 10 during winter showed completely uniqueabiotic and biotic characteristics: the sedimentswere dominated by the fine sand fraction and hadmedium organic matter content, no metal anthro-pogenic contamination was observed, and the sitepresented the lowest total abundance and diver-sity values and the highest evenness index.

The group G2 (summer, autumn and winter:sites 2 and 3; autumn-site 4; summer-site 10) wasformed with a mean similarity of 34.47 % andrepresented 41.29 % of the total abundance; the

dominant species Cyathura carinata contributed44.68 % to this cluster. Almost all of the sitesof this group are located along the Coura Rivermainstream, with sediments dominated by graveland very coarse sand, low organic matter contentsand low metal concentrations, but all had hightotal abundances and low evenness indices. Thiscluster can be considered as the most species-richmacrobenthic group of the saltmarsh.

The group G3 (summer: sites 5, 6 and 8; au-tumn: sites 5, 6, 8 and 10; winter: sites 6 and 8)was formed with a mean similarity of 36.78 %and represented 31.32 % of the total abundance;Scolelepis squamata contributed 32.37 % to thegroup. This group is formed by sites located inthe interior areas of the saltmarsh, and their finersediments, higher organic matter contents andsome evidence of metal contamination are cou-pled with low macrobenthic abundances and di-versities and high evenness indices.

Finally, group G4 (summer: sites 1, 4, 7, 9 and10; autumn: sites 1, 7 and 9; winter: sites 1, 4,5, 7 and 9) was formed with a mean similarityof 39.86 % and represented 25.00 % of the to-tal abundance of the macrobenthic community;Hediste diversicolor contributed 59.57 %. Thislast cluster grouped sites with different abiotic(sediments with high reductions of finer fractionsand organic matter contents from summer to au-tumn and winter, as well as both contaminatedand uncontaminated sediments) and biotic (siteswith high and low numbers of species, Shannon-Wiener diversity values and evenness indices)characteristics.

These cluster multivariate analyses suggestedthat in cases of acute contamination associatedwith the death of macrobenthic communities, theareas of group G1 may suffer greater negative en-vironmental impacts while those of groups G2–G4 will adapt more readily to the new environ-mental conditions.

However, the principal component analysis(PCA) based on the biotic and abiotic data fromthe two most different hydrological conditions(Su: Summer and W: Winter) obtained only threeclusters of sampling sites (A, B and C) (Fig. 3).This PCA explained a total of 76.07 % of the datavariability and showed the same positive correla-


84 Picanço et al.

tions between the sampling sites with finer sed-iment fractions and metal concentrations. PC1

(explaining a total of 51.90 % of the data vari-ability) was positively influenced by the coarsersediment fractions and negatively impacted bythe very fine sand, silt and clay fractions, or-ganic matter contents and metal concentrations.PC2 explained only 24.17 % of the data variabil-ity and was associated with the biotic character-istics of the macrobenthic communities.

Furthermore, the BIO-ENV analysis (Spear-man Coefficient) used to study the influence ofthe abiotic variables in the biotic ecosystemsrevealed that the texture of the sediments wasthe most important variable to the macrobenthiccommunity structure, particularly the fine sandfraction (ρ = 0.311) and organic matter contents(ρ = 0.261) (Table 4). Even when BIO-ENVcombined more than one variable, the metal con-centrations in the sediments were never shown as asignificant “best variable combination” (Table 4).

The comparison of the 4 faunal groups (G1,G2, G3 and G4) formed by the “cluster multi-variate analysis” and the 3 abiotic groups (A, Band C) formed by the PCA confirmed that thegroup distributions were not the same, althoughsome sites remained associated. This result sug-

gested that macrobenthic community structureof the Minho estuary saltmarsh was not directlyinfluenced by metals. The presence of high metalconcentrations might be considered as a simpledisturbing factor. Although the saltmarsh showedevidence of anthropogenic contamination bymetals, the texture of the sediments was the mainstructuring factor of the area’s macrobenthiccommunity.

CONCLUSIONS

The texture and organic matter contents of thesediments showed high spatial and seasonalvariations across the Minho estuary saltmarshfor the three sampling dates, which demon-strated their complex sedimentary dynamics.The metal concentrations of the sediments alsoshowed significant spatial and seasonal vari-ations ( p < 0.05), which coincided with thevariations in texture and organic matter contentsbetween sampling sites and seasons. However,the metal concentrations in the sediments werenot exclusively influenced by natural sources,showing evidence of anthropogenic contami-nation in the saltmarsh’s interior areas during

-8 -6 -4 -2 0 2 4 6

PC1

-3,0

-2,5

-2,0

-1,5

-1,0

-0,5

0

0,5

1,0

1,5

2,0

2,5

3,0

PC

2

Su1

Su2

Su3

Su4

Su5Su6

Su7

Su8

Su9

Su10

W1

W2

W3

W4

W5

W6

W7

W8

W9

W10

Figure 3. Principal Component Analysis (PCA) of the biotic and abiotic factors of the sediments of the Minho estuary saltmarshduring the two extreme hydrological conditions: Summer (Su) and Winter (W). Análisis de Componentes Principales (PCA) de los

factores bióticos y abióticos de los sedimentos del estuario del río Miño, durante dos condiciones hidráulicas extremas: verano (Su)

e invierno (W).



summer (sites 5 and 7) and winter (site 5).The macrobenthic community structure of thissaltmarsh was composed of a total of 37 taxa.The mean annual abundance was 1530 ind/m2,and the most abundant species were Cyathura

carinata, Scolelepis squamata and Hediste

diversicolor. However, these species showedno consistent variation across the saltmarsh,and their abundances and diversities displayedhigh spatial and seasonal variations directlyinfluenced by the natural characteristics of thesediments and the environmental conditionstypical of each season. Although the saltmarshshowed evidence of anthropogenic contamina-tion by metals, the main structuring factor ofits macrobenthic community was the texture ofthe sediments. The evidence of anthropogeniccontamination by metals should be furtherstudied and included in periodic ecologicalmonitoring and remediation programs for theMinho estuary saltmarsh. Additionally, it mustbe stressed that these preliminary results shouldbe strengthened with more complete monitoringprograms and comparisons with macrobenthiccommunity structures from different nationaland international saltmarshes.

REFERENCES

ATTRILL, M. J., S. D. RUNDLE & R. M. THOMAS.1996. The influence of drought-induced low fresh-water flow on an upper-estuarine macroinverte-brate community. Water Research, 30: 261–268.

ALVES, A. M. 1996. Causas e processos da dinâmica

sedimentar na evolução actual do litoral do Alto

Minho. PhD Thesis in Sciences, Department ofEarth Sciences, University of Minho.

ALVES, E. 2000. Plano de Bacia Hidrográfica do

rio Minho: Análise e Diagnóstico da Situação Ac-

tual. Anexo 11-Situações Hidrológicas Extremas-Cheias. Relatory N.o53/00-NHE, Lisbon, LNEC,25-29.APHA. 1998. Standard Methods for the Ex-

amination of Water and Wastewater. Section: In-

trodution; Method: 1030C-Data Quality. 20th edi-tion. American Public Health Association, Wash-ington, DC.

ASENSIO, A. I. & M. M. J. GÓMEZ. 1984. Ocea-nografía física: Factores que condicionan la diná-

mica litoral en la Ría del Eo. Issue from Galician

Studies Seminary, 79–90.BRUYNDONCX, L, K. JORDAENS, T. YSEBAERT,

P. MEIRE & T. BACKELJAU. 2002. Molluscandiversity in tidal marshes along the Scheldt estuary(The Netherlands, Belgium). Hydrobiologia, 474:189–196.

CANFIELD, T. J., N. E. KEMBLE, W. G. BRUM-NAUGH, F. J. DWYER, J. F. INGERSOLL &C. G. FAIRCHILD. 1994. Use of benthic inver-tebrates community structure and the SedimentQuality Triad to evaluate metal-contaminatedsediment in the upper Clark Fork River, Montana.Environmental Toxicology and Chemistry, 13:1999–2012.

CHAPMAN, P. M. & F. WANG. 2001. Assesing sed-iment contamination in estuaries. Environmental

Toxicology and Chemistry, 20: 3–22.CLARKE, K. & R. GORLEY. 2001. PRIMER v5 -

User manual/Tutorial. Plymouth, PRIMER-E Ltd.CLARKE, K. R. & R. M. WARWICK. 1994. Changes

in marine communities: an approach to statistical

analysis and interpretation. Plymouth, Natural En-vironmental Research Council.

COSTA-DIAS, S., V. FREITAS, R. SOUSA & C.ANTUNES. 2010. Factors influencing epiben-thic assemblages in the Minho Estuary (NWIberian Peninsula). Marine pollution bulletin, 61:240–246.

DAY, J. W., C. A. S. HALL, W. M. KEMP & A.YÁNEZ-ARANCIBIA. 1989. Estuarine Ecology.New York, Wiley - Interscience Publication.

DAUVIN, J. C. 2007. Paradox of estuarine quality:benthic indicators and indices, consensus or debatefor the future. Marine Pollution Bulletin, 55: 271–281.DIEZ, J. 1980. Introducción al estudio geo-morfológico y de los procesos litorales en la Ríade Foz. Issue from Galician Public Building Rela-

tory, 941–952.ELLIOTT, M. & V. M. QUINTINO. 2007. The Estu-

arine Quality Paradox, Environmental Homeosta-sis and the difficulty of detecting anthropogenicstress in naturally stressed areas. Marine Pollution

Bulletin, 54: 640–645.EPA-U.S. ENVIRONMENTAL PROTECTION AGEN-

CY. 1994. Method 3051-Microwave assisted acid

digestion of sediments, sludges and soils. TestMethods for Evaluating Solid Waste, SW-846,3rd ed., Office of Solid Waste and EmergencyResponse of Washington, D.C.


86 Picanço et al.

FARINHA, J. C. & A. TRINDADE. 1994. Contri-

buição para o Inventário e Caracterização de

Zonas Húmidas em Portugal Continental. Portu-guese Institute of Nature Conservation (ICN)/MedWet Publication.

GAMBOA, M. 1999. Plano de Bacia Hidrográfica

do rio Minho: Análise e Diagnóstico da Situação

Actual. Anexo 1 - Análise Biofísica, Parte III-Clima. Relatory N.o 318/99-GHi, Lisbon, LNEC.

GASTON, G. R. & J. C. NASCI. 1998. Trophic struc-ture of macrobenthic communities in the CalcasieuEstuary, Louisiana. Estuaries, 3: 201–211.

LAMBSHEAD, P. J. D., H. M. PLATT & K. M.SHAW. 1983. The detection of differences amongassemblages of marine benthic species based onan assessment of dominance and diversity. Journal

of Natural History, 17: 859–874.LANA, P. C. 1994. Organismos bénticos e actividades

de monitoramento. Issue In: Biological Oceanog-

raphy. Oceanic and Coastal Environmental Diag-

nostic from South and Southeast regions of Brazil,PETROBRÁS-FUNDESPA: 10–21.

MIL-HOMENS, M., A. M. COSTA, S. FONSECA,M. A. TRANCOSO, C. LOPES, R. SERRANO& R. SOUSA. 2013a. Characterization of heavy-metal contamination in surface sediments of theMinho river estuary by way of factor analysis.Archives of environmental contamination and tox-

icology, 64: 617–631.MIL-HOMENS, M., A. M. COSTA, S. FONSECA,

M.A. TRANCOSO, C. LOPES, R. SERRANO &R. SOUSA. 2013b. Natural heavy metal and met-alloid concentrations in sediments of the MinhoRiver estuary (Portugal): baseline values for envi-ronmental studies. Environmental monitoring and

assessment, 185: 5937–5950.MORA, J. 1980. Poblaciones bentônicas de la Ría de

Arosa. PhD Thesis, Biology Faculty, University ofSantiago de Compostela.

MUCHA, A. P., M. T. S. D. VASCONCELOS & A.A. BORDALO. 2003. Macrobenthic communityin the Douro estuary: relations with trace metalsand natural sediments characteristics. Environmen-

tal Pollution, 121: 169–180.PEARSON, T. H. & R. ROSENBERG. 1978.

Macrobenthic succession in relation to organicenrichment and pollution of marine environment.Oceanography and Marine Biology: An Annual

Review, 16: 229–311.RAKOCINSKI, C. F., S. S. BROWN, G. R. GAS-

TON, R. W. HEARD, W. W. WALKER & J. K.

SUMMERS. 1997. Macrobenthic responses to nat-ural and contaminant-related gradients in northernGulf of Mexico estuaries. Ecological Applications,7: 1278–1298.

REIS, P. A., J. C. ANTUNES & C. M. R. ALMEIDA.2009. Metal levels in sediments from the Minhoestuary salt marsh: a metal clean area? Environ-

mental Monitoring and Assessment, 159: 191–205.RUNDLE, S. D, M. J. ATTRILL & A. ARSHAD.

1998. Seasonality in macroinvertebrates commu-nity composition across a neglected ecologicalboundary, the freshwater-estuarine transition zone.Aquatic Ecology, 32: 211–216.

SCHIFF, K. C. & S. B. WEISBERG. 1999. Iron as areference element for determining trace metal en-richment in southern California coastal shelf sedi-ments. Marine Environmental Research, 48: 161–176.

SOUSA, R., S. DIAS, V. FREITAS & C. ANTUNES.2008. Subtidal macrozoobenthic assemblagesalong the River Minho estuarine gradient (north-west Iberian Peninsula. Aquatic Conservation:

Marine and Freshwater Ecosystems, 18: 1063–1077.

SOUSA, C. M., N. VAZ, I. ALVAREZ & J. M. DIAS.2013. Effect of Minho estuarine plume on RiasBaixas: numerical modeling approach. Journal of

Coastal Research, Special Issue 65: 2059–2065.TEAL, J. M. 1986. The ecology of regularly flooded

salt marshes of New England: A community pro-file. Fish and Wildlife Service, Division of Biolog-ical Services, Washington. D. C. Biology Report,85: 77.

VALE, C., F. M. CATARINO, C. CORTESÃO & M.I. CAÇADOR. 1990. Presence of metal-rich rhizo-concretions on the roots of Spartina maritima fromthe salt marshes of the Tagus estuary, Portugal. Sci-

ence of Total Environment, 98: 617–626.VASCONCELOS, V., & M. CERQUEIRA. 2001.

Phytoplankton community of river Minho (Inter-national Section). Limnetica, 20: 135–141.

VELINSKY, D. J., T. L. WADE, C. E. SCHLEKAT,B. L. MCGEE & B. J. PRESLEY. 1994. Tidalriver sediments in the Washington D. C. Area. I.Distribution and sources of trace metals. Estuaries,17: 305–320.

WARWICK, R. M. 1986. A new method for detect-ing pollution effects on marine macrobenthic com-munties. Marine Biology, 92: 557–562.

WEISBERG, S. B., J. A. RANASINGUE, D. M.DAUER, L. C. SCAFFNER, R. J. DIAZ & J. B.



FRITHSEN. 1997. An estuarine benthic indexof biotic integrity (B-IBI) for Chesapeake Bay.Estuaries, 20: 149–158.

YSEBAERT, T., P. MEIRE, P. M. J. HERMAN & H.

VERBEEK. 2002. Macrobenthic species responsesurfaces along estuarine gradients: prediction bylogistic regression. Marine Ecology Progress Se-

ries, 225: 79–95.


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